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BIROn - Birkbeck Institutional Research Online
Brewer, Rebecca and Biotti, Federica and Bird, Geoffrey and Cook, Richard(2017) Typical integration of emotion cues from bodies and faces in AutismSpectrum Disorder. Cognition 165 , pp. 82-87. ISSN 0010-0277.
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In press at Cognition
Format: Brief article
Running head: Integration of body and face cues in autism
Typical integration of emotion cues from bodies and faces in
Autism Spectrum Disorder
Rebecca Brewer1, Federica Biotti
2, Geoffrey Bird
3,4,5, & Richard Cook
2
1Department of Psychology; Royal Holloway, University of London
2Department of Psychology; City, University of London
3Institute of Cognitive Neuroscience; University College London
4Experimental Psychology Department; University of Oxford
5MRC Social, Genetic & Developmental Psychiatry Centre; King’s College London
*Corresponding author:
Department of Psychology
Royal Holloway, University of London
Egham Hill, Egham,
Surrey, UK, TW20 0EX
Key words: Autism Spectrum Disorder; Social Perception;
Contextual Modulation; Emotion recognition; Body posture
2
Highlights
Cues to another’s emotion are automatically integrated across the face and body
We tested integration of face and body emotion cues in Autism Spectrum Disorder
Integration of face and body emotion cues in individuals with autism was typical
Reliance on body cues was greatest in those with poor facial emotion classification
3
Abstract
Contextual cues derived from body postures bias how typical observers categorize facial
emotion; the same facial expression may be perceived as anger or disgust when aligned with
angry and disgusted body postures. Individuals with Autism Spectrum Disorder (ASD) are
thought to have difficulties integrating information from disparate visual regions to form
unitary percepts, and may be less susceptible to visual illusions induced by context. The
current study investigated whether individuals with ASD exhibit diminished integration of
emotion cues extracted from faces and bodies. Individuals with and without ASD completed
a binary expression classification task, categorizing facial emotion as ‘Disgust’ or ‘Anger’.
Facial stimuli were drawn from a morph continuum blending facial disgust and anger, and
presented in isolation, or accompanied by an angry or disgusted body posture. Participants
were explicitly instructed to disregard the body context. Contextual modulation was inferred
from a shift in the resulting psychometric functions. Contrary to prediction, observers with
ASD showed typical integration of emotion cues from the face and body. Correlation
analyses suggested a relationship between the ability to categorize emotion from isolated
faces, and susceptibility to contextual influence within the ASD sample; individuals with
imprecise facial emotion classification were influenced more by body posture cues.
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1. Introduction
The facial expressions of others are a rich source of social information, conveying cues to
affective and mental states. Correct interpretation of facial expressions is therefore important
for fluent social interaction and wider socio-cognitive development (Adolphs, 2002; Frith,
2009). Previous research indicates that facial emotion perception is affected by the context in
which a facial expression is encountered, suggesting that interpretations are informed by our
knowledge and experience (de Gelder et al., 2006; Feldman-Barrett, Mesquita, & Gendron,
2011). Categorization of morphed facial expressions, for example, is biased by the concurrent
presentation of social interactants (Gray, Barber, Murphy, & Cook, 2017) and other non-
interacting faces (Masuda et al., 2008). Perceived facial expression can also be influenced by
affective vocal cues (de Gelder & Vroomen, 2000; Massaro & Egan, 1996), situational stories
(Carroll & Russell, 1996), and visual scenes (Righart & De Gelder, 2008a, 2008b).
A particularly strong form of contextual influence is exerted by body postures (Hassin,
Aviezer, & Bentin, 2013). The same facial expression can vary in appearance when presented
with different bodily expressions; for example, a facial expression may be classified as angry
when presented in the context of a body expressing anger, but disgusted when presented in
the context of a body expressing disgust (Aviezer et al., 2008; Aviezer, Trope, & Todorov,
2012b). These findings imply that the attribution of affective states involves the integration of
emotion cues from across the face and body. The influence of posture contexts is often
automatic; it occurs despite explicit instructions to disregard non-face information (Aviezer,
Bentin, Dudarev, & Hassin, 2011), and modulates early neurophysiological markers of visual
person processing (Meeren, van Heijnsbergen, & de Gelder, 2005).
The present study sought to examine whether observers with Autism Spectrum Disorder
(ASD) integrate emotion cues from body posture contexts when interpreting others’ facial
emotion. ASD is a neurodevelopmental condition associated with social and communication
difficulties, repetitive behaviors and restricted routines (American Psychiatric Association,
2013). There has been considerable interest in the visual perception of individual with ASD
(Dakin & Frith, 2005; Simmons et al., 2009). Observers with ASD may exhibit a local
processing style that hinders their ability to form unified global percepts (Behrmann, Thomas,
& Humphreys, 2006; Happé, 1999; Happé & Frith, 2006). For example, ASD is associated
with good detection of embedded figures, which requires observers to disregard extraneous
5
information present within a complex pattern or scene, to locate a target element (Ropar &
Mitchell, 2001; Shah & Frith, 1983). Those with ASD may also be less susceptible to
context-induced visual illusions than typical individuals (Happé, 1996; Shah, Bird, & Cook,
2016; but see Manning, Morgan, Allen, & Pellicano, 2017) and show reduced global-to-local
interference when responding to (“Navon”) compound letter arrays (Behrmann, Avidan et al.,
2006). Similarly, individuals with ASD may rely less than typical individuals on contextual
cues to distinguish homographs when reading (Frith & Snowling, 1983; López & Leekam,
2003).
Should observers with ASD exhibit a local processing style, their judgements of facial
emotion may be less susceptible to modulation by body posture contexts. Where observed,
aberrant integration of emotion cues from bodies and faces may contribute to difficulties
attributing affective states sometimes seen in this population (Gaigg, 2014). Observers with
ASD and matched control participants were required to classify expressions drawn from a
morph continuum as either ‘Anger’ or ‘Disgust’. Target expressions were either judged in a
no-context baseline condition, in the presence of a task-irrelevant disgusted posture, or a task-
irrelevant angry posture.
2. Method
2.1 Participants
Nineteen individuals with a clinical diagnosis of ASD (three female; Mage = 34.84 years), and
27 individuals with no current or previous clinical diagnosis (eight female; Mage = 33.85
years) took part in the current study. All participants were aged between 18 and 65 years.
Typical participants were recruited from local participant pools populated by university
students and members of the general public. ASD participants were recruited from a database
maintained by the authors. Individuals with ASD were diagnosed by an independent
clinician, and the Autism Diagnostic Observation Schedule (ADOS; Lord et al., 2000) was
used to assess current severity. Autistic traits were also measured in all participants using the
Autism-Spectrum Quotient (AQ; Baron-Cohen, Wheelwright, Skinner, Martin, & Clubley,
2001). Higher AQ scores, indicative of more ASD traits, were seen in the ASD group than in
the typical group [t(44) = 7.28, p < .001]. Alexithymia, a trait associated with difficulties
identifying and describing one’s own emotions (Brewer, Cook, & Bird, 2016a, 2016b),
measured by the Toronto Alexithymia Scale (TAS-20; Bagby, Taylor, & Parker, 1994), was
6
also more severe in the ASD group (M = 59.16, SD = 15.81) than the typical group (M =
46.58, SD = 12.77) [t(43) = 2.95, p = .005]. However, the ASD and typical groups did not
differ significantly in their age [t(44) = .27, p = .787], proportion of female participants [X2 =
.13, p = .248], or IQ [t(43) = 1.032, p = .308]. Detailed diagnostic information is provided in
Table 1.
Table-1
2.2 Stimuli
Facial stimuli (Figure 1a) were static images drawn from a morph continuum created by
blending two images of the same actor expressing disgust and anger (images taken from
Ekman & Friesen, 1975) using Morpheus Photo Morpher Version 3.11 (Morpheus Software,
Inc). The continuum parametrically manipulated the actor’s expression between disgust and
anger in seven equidistant steps of 10%. The body contexts depicted the same actor posing
angry and disgusted postures (Figure 1b). Where these posture contexts have been used
previously (e.g., Aviezer et al., 2008; Aviezer et al., 2012b), the disgusted body posture has
been shown gripping a disgusting object. In the present study, this object was removed to
ensure that perceptual bias, where observed, was attributable to integration of face and body
cues, and not additional semantic information. The morphed facial expressions were
presented within a dark grey oval intended to resemble a hood. The relative location of the
facial target did not vary as a function of expression intensity. In the baseline no-context
condition, observers saw the expressions presented within the oval, but in the absence of a
body posture. We opted for this baseline condition in light of concerns about the value of the
neutral emotion construct (e.g., Lee, Kang, Park, Kim, & An, 2008); for example, a
supposedly “neutral” body posture, where an actor’s arms are clenched by their side, may be
perceived as angry. In all three conditions, facial stimuli subtended 3.5° vertically when
viewed at 57 cm.
Figure-1
2.3 Procedure
Each trial in the experimental procedure began with a central fixation point (1000 ms),
followed by presentation of a facial target drawn from the morph continuum (1200 ms). The
7
facial target was always presented centrally. In the baseline no-context condition, the facial
target was presented in isolation. In the two context conditions, the facial target was
accompanied by an angry or disgusted body posture. Following stimulus offset, participants
were prompted to categorize the facial emotion as either ‘Disgust’ or ‘Anger’ using a key
press. Participants were explicitly instructed to disregard the body context. The procedure
consisted of 420 trials (7 facial stimuli × 20 presentation × 3 context conditions) and was
presented on an LCD display. Stimuli were presented in a randomized order, with the three
context conditions interleaved. The experimental program was written in MATLAB (The
MathWorks, Inc) using the Psychophysics Toolbox (Brainard, 1997; Pelli, 1997).
For each observer, we fitted separate psychometric functions for the three context conditions,
each modelling how the probability of a disgust response varied as a function of the strength
of the disgust signal in the stimulus. Cumulative Gaussian functions were fitted using the
Palamedes toolbox (Prins & Kingdom, 2009). Each function estimated two key parameters:
Decision noise and the point of subjective equality (PSE). Decision noise is a measure of the
precision with which stimuli are categorized, defined as the standard deviation of the
symmetric Gaussian distribution underlying each cumulative Gaussian function. Lower noise
estimates indicate that observers can perceive subtle differences in stimulus strength and vary
their responses accordingly. Greater noise estimates reveal that participants’ responses are
relatively invariant to changes in stimulus strength. Noise estimates are inversely related to
the slope of the psychometric function; steep and shallow slopes are associated with low and
high noise estimates, respectively. The PSE is a measure of bias that represents the
hypothetical emotion intensity equally likely to be judged as ‘Disgust’ and ‘Anger’.
Observers’ susceptibility to the contextual modulation was inferred from the difference
between PSE of the anger function and the PSE of the disgust function (Figure 1c).
3. Results
One individual in the ASD group (participant 19) produced psychometric functions that could
not be modeled so was excluded from all analyses. Goodness-of-fit was evaluated by
calculating deviance scores for each function (McCullagh & Nelder, 1989). In general, fits
were good in both groups; deviance scores (whereby lower deviance indicates better fit) for
those with (M = 6.97, SD = 8.55) and without (M = 8.85, SD = 7.44) ASD did not differ
significantly in the baseline no-context condition [t(43) = .781, p = .439].
8
Figure-2
First, we examined the decision noise of the two groups (Figure 2a). The ASD (M = 15.0%,
SD = 13.9%) and typical (M = 11.7%, SD = 5.94%) groups did not differ significantly with
respect to decision noise in the baseline no-context condition [t(43) = .968, p = .344],
suggestive of broadly comparable emotion recognition. However, the ASD group exhibited
greater variability in decision noise than the typical group (Levene’s F = 9.97, p = .003).
Next, we examined the groups’ susceptibility to the contextual modulation (Figure 2b).
Significant contextual modulation (shifts > 0%) was observed in both the ASD [t(17) = 2.50,
p = .023] and typical [t(26) = 3.43, p = .002] groups. Furthermore, the ASD (M = 7.73%, SD
= 12.9%) and typical (M = 3.47%, SD = 5.26%) groups did not differ in their susceptibility to
the contextual modulation [t(43) = 1.30, p = .207], although modulation was numerically
greater in the ASD group. The ASD and typical groups were also comparable in terms of
their baseline decision noise [t(36) = 1.24, p = .234] and their susceptibility to the contextual
modulation [t(36) = 1.17, p = .261] when participants of 50 years-of-age or over were
excluded (four participants in each group).
Correlation analyses (Figure 2c) conducted on the combined sample of 45 observers revealed
a significant positive association between decision noise in the baseline no-context condition,
and susceptibility to the contextual modulation [r = .63, p < .001]. Participants who exhibited
imprecise classification of isolated facial expressions exhibited greater contextual
modulation. When the ASD and typical groups were separated, this association remained
significant in the ASD group [r = .73, p < .001], even when an outlier with a large context
effect (participant 17 of the ASD sample) was removed [r = .74, p = .001]. This correlation
did not reach significance in the typical group [r = .19, p = .333]. A Fisher r-to-z test
indicated that the strength of the correlation was significantly greater in the ASD than the
typical group [z = 2.22, p = .026].
ADOS score was not significantly correlated with either contextual modulation (r = .03, p =
.901) or decision noise in the baseline no-context condition (r = -.01, p = .983). In the sample
as a whole, AQ scores correlated with context induced PSE shift (r = .32, p = .035), whereby
presence of more ASD traits was associated with greater PSE shifts, but this correlation did
9
not remain significant when participant 17 was removed (r = .18, p = .237). AQ scores were
not associated with decision noise in the baseline no-context condition (r = .15, p = .322).
TAS-20 scores were not significantly correlated with contextual modulation (r = .03, p =
.856) or baseline decision noise (r = -.02, p = .904).
4. Discussion
The current study investigated whether individuals with and without ASD differ in the extent
to which body posture contexts influence interpretation of emotional facial expressions.
Despite explicit instructions to disregard the context, the presence of the body postures biased
observers’ categorization of facial emotion; expressions were more likely to be judged as
angry and disgusted when aligned with angry and disgusted bodies, respectively. Contrary to
prediction, however, participants with and without ASD were influenced to a similar degree
by emotional cues present in the body contexts.
Previous studies indicate that individuals with ASD are less susceptible to contextual effects
in a range of domains (e.g., Behrmann, Avidan et al., 2006; Happé, 1996; López & Leekam,
2003; Ropar & Mitchell, 2001), leading to the view that ASD is associated with difficulties
forming integrated percepts (Behrmann, Thomas et al., 2006; Happé, 1999; Happé & Frith,
2006) and problems using context to inform perceptual inference (Lawson, Rees, & Friston,
2014; Palmer, Lawson, & Hohwy, 2017). Our finding that body contexts bias perception of
facial emotion in observers with ASD is not consistent with this characterisation of ASD. The
reason for this apparent disparity warrants further investigation. In typical observers,
integration of bodily and facial cues likely emerges in response to covariation of facial and
bodily expressions. It is possible that adults with ASD have sufficient visual experience of
these contingencies to develop typical integration mechanisms, despite a local processing
style. Reduced attention to faces (Dawson, Webb, & McPartland, 2005; Klin, Jones, Schultz,
Volkmar, & Cohen, 2002; Nakano et al., 2010) may also promote greater reliance on bodily
cues in this population.
We observed striking variation in expression categorization ability in our ASD sample. While
some members of the ASD group exhibited categorization performance comparable with the
best typical participants, three performed at least two standard deviations below the typical
mean. This adds further weight to the emerging view that deficits of facial expression
10
perception in ASD are weak and inconsistent at the group level (Harms, Martin, & Wallace,
2010; Lozier, Vanmeter, & Marsh, 2014; Uljarevic & Hamilton, 2013). Indeed, one
influential review concluded that “behavioral studies are only slightly more likely to find
facial emotion recognition deficits in autism than not” (Harms et al., 2010, p317). While is it
undeniable that some individuals within the ASD population experience difficulties
recognizing facial emotion, these deficits do not appear to be a universal feature of this
condition, and may instead reflect co-occurring conditions such as alexithymia (Bird & Cook,
2013; Cook, Brewer, Shah, & Bird, 2013).
Interestingly, the susceptibility of those with ASD to contextual modulation was related to
their performance when judging the facial expressions in isolation; observers with imprecise
expression categorization in the no-context condition were influenced more by the body
posture contexts when present. A similar trend was observed in the typical group, however
this correlation did not reach significance, possibly due the limited variability in baseline
decision noise in this sample (e.g., Howitt & Cramer, 2009). While correlations inferred from
small samples must be treated with caution (Schönbrodt & Perugini, 2013), the suggestion
that stimulus ambiguity and contextual influence are closely linked, accords with current
thinking about the role of context in human vision (Bar, 2004; Friston, 2005; Gilbert & Li,
2013; Gregory, 1997). When target stimuli are unmistakable, observers may distinguish
between different perceptual hypotheses without reference to the context. When the physical
attributes of a target stimulus do not clearly distinguish between different perceptual
hypotheses, however, contextual information may be weighted more strongly to resolve the
ambiguity. This view also fits well with the finding that physically similar facial expressions
associated with intense positive and negative emotions (Aviezer, Trope, & Todorov, 2012a),
or created by image morphing (Van den Stock, Righart, & De Gelder, 2007), are particularly
receptive to contextual influence from body postures.
Some readers may be concerned that participants with poor facial emotion recognition chose
to ignore the facial cues entirely, and responded to bodily emotion instead. Crucially, any
attempt to treat the current procedure as a bodily expression recognition task would yield
responses that failed to vary as a function of facial expression intensity. All but one
participant (who was excluded from all analyses), however, produced monotonic
classification functions that could be modelled using a cumulative Gaussian.
11
In conclusion, the current findings suggest that individuals with ASD and typical observers
show broadly comparable integration of emotion cues from faces and bodies. Consistent with
previous studies, individuals with ASD differed widely in their baseline ability to classify
facial expressions. Correlation analyses suggested a relationship between ability to categorise
emotion when faces were presented in isolation, and susceptibility to contextual influence;
those observers with ASD who exhibited imprecise categorization in the baseline condition
were influenced more by body posture contexts. This finding accords with the view that the
visual system weights contextual information strongly when interpreting ambiguous stimuli.
12
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Simmons, D. R., Robertson, A. E., McKay, L. S., Toal, E., McAleer, P., & Pollick, F. E.
(2009). Vision in autism spectrum disorders. Vision Research, 49, 2705-2739.
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recognition of emotions in the face and voice. Emotion, 7, 487-494.
18
Figures
Figure 1
Figure 1. (a) Facial expressions were drawn from a morph continuum that blended anger and disgust emotions
in 10% increments. (b) The facial expressions were either presented in isolation (no context) or aligned with
angry and disgusted body postures. (c) An observer’s susceptibility to the contextual modulation was inferred
from the difference between the PSE of their disgusted function and the PSE of their angry function.
19
Figure 2
Figure 2. (a) Decision noise and (b) PSE estimates for the ASDs and the typical observers in the three
conditions. (c) Scatterplot of the correlation between baseline decision noise and susceptibility to the contextual
modulation.
20
Tables
Table 1. Autism Diagnostic Observational Schedule (ADOS) classification and total score, Autism Quotient
Score, and Full-Scale IQ score for all participants in the ASD group. Mean AQ, IQ, and TAS-20 scores for
typical participants are shown below. Note: one typical individual did not complete the TAS-20, and one did not
complete the IQ assessment.
Participant ADOS Classification ADOS Gender Age AQ Full-Scale IQ TAS-20
1 Autism Spectrum 7 Male 61 45 132 61
2 Autism 10 Male 35 46 112 54
3 Autism 10 Female 22 20 121 44
4 Autism 11 Male 31 37 118 38
5 Autism Spectrum 8 Male 18 21 107 73
6 Autism Spectrum 7 Male 38 40 116 71
7 Autism Spectrum 7 Male 38 17 125 27
8 Autism Spectrum 8 Male 35 36 108 72
9 Autism 14 Male 50 50 121 84
10 Autism Spectrum 9 Male 19 31 92 60
11 Autism 12 Male 31 48 107 64
12 Autism 15 Female 52 45 116 69
13 Autism 15 Male 52 27 118 41
14 Autism 10 Male 21 35 107 72
15 Autism 11 Male 42 33 117 36
16 Autism Spectrum 9 Male 25 39 133 61
17 Autism Spectrum 8 Female 21 46 93 81
18 Autism Spectrum 9 Male 33 35 128 60
19 Autism 14 Male 38 23 78 56
ASD mean
(SD)
34.84
(12.46)
35.47
(10.14)
113.11
(14.03)
59.16
(15.81)
Typical mean
(SD)
33.85
(11.92)
16.93
(5.42)
108.73
(14.06)
46.58
(12.77)